Lipid and carotenoid cooperation-driven adaptation to light and temperature stress in Synechocystis sp. PCC6803

Biochim Biophys Acta Bioenerg. 2017 May;1858(5):337-350. doi: 10.1016/j.bbabio.2017.02.002. Epub 2017 Feb 8.

Abstract

Polyunsaturated lipids are important components of photosynthetic membranes. Xanthophylls are the main photoprotective agents, can assist in protection against light stress, and are crucial in the recovery from photoinhibition. We generated the xanthophyll- and polyunsaturated lipid-deficient ROAD mutant of Synechocystis sp. PCC6803 (Synechocystis) in order to study the little-known cooperative effects of lipids and carotenoids (Cars). Electron microscopic investigations confirmed that in the absence of xanthophylls the S-layer of the cellular envelope is missing. In wild-type (WT) cells, as well as the xanthophyll-less (RO), polyunsaturated lipid-less (AD), and the newly constructed ROAD mutants the lipid and Car compositions were determined by MS and HPLC, respectively. We found that, relative to the WT, the lipid composition of the mutants was remodeled and the Car content changed accordingly. In the mutants the ratio of non-bilayer-forming (NBL) to bilayer-forming (BL) lipids was found considerably lower. Xanthophyll to β-carotene ratio increased in the AD mutant. In vitro and in vivo methods demonstrated that saturated, monounsaturated lipids and xanthophylls may stabilize the trimerization of Photosystem I (PSI). Fluorescence induction and oxygen-evolving activity measurements revealed increased light sensitivity of RO cells compared to those of the WT. ROAD showed a robust increase in light susceptibility and reduced recovery capability, especially at moderate low (ML) and moderate high (MH) temperatures, indicating a cooperative effect of xanthophylls and polyunsaturated lipids. We suggest that both lipid unsaturation and xanthophylls are required for providing the proper structure and functioning of the membrane environment that protects against light and temperature stress.

Keywords: Cyanobacteria; Lipid remodeling; Lipid-carotenoid-protein interactions; Photoinhibition; Temperature stress; Xanthophylls.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adaptation, Physiological
  • Cell Membrane / genetics
  • Cell Membrane / metabolism
  • Cell Membrane / radiation effects*
  • Cell Membrane / ultrastructure
  • Genotype
  • Light*
  • Lipid Metabolism / genetics
  • Lipid Metabolism / radiation effects
  • Membrane Lipids / metabolism
  • Membrane Lipids / radiation effects*
  • Mutation
  • Phenotype
  • Photosynthesis / genetics
  • Photosynthesis / radiation effects*
  • Photosystem I Protein Complex / genetics
  • Photosystem I Protein Complex / metabolism
  • Photosystem I Protein Complex / radiation effects*
  • Stress, Physiological*
  • Synechocystis / genetics
  • Synechocystis / metabolism
  • Synechocystis / radiation effects*
  • Synechocystis / ultrastructure
  • Temperature*
  • Thylakoids / metabolism
  • Thylakoids / radiation effects
  • Time Factors
  • Xanthophylls / genetics
  • Xanthophylls / metabolism
  • Xanthophylls / radiation effects*
  • beta Carotene / metabolism
  • beta Carotene / radiation effects

Substances

  • Membrane Lipids
  • Photosystem I Protein Complex
  • Xanthophylls
  • beta Carotene